Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: Angular torque profile of the enzyme

ATP synthase (FOF1) operates as two rotary motor/generators coupled by a co mmon shaft. Both portions, F-1 and F-O, are rotary steppers. Their symmetri es are mismatched (C-3 versus C10-14). We used the curvature of fluorescent actin filaments, attached to the rotating c-ring, as a spring balance (fle xural rigidity of 8 (.) 10(-26) Nm(2)) to gauge the angular profile of the output torque at F-O during ATP hydrolysis by F-1 (see theoretical companio n article (Cherepanov, D. A., and W. Junge, 2001. Biophys. J. 81:1234-1244. )). The large average output torque (50 +/- 6 pN (.) nm) proved the absence of any slip. Variations of the torque were small, and the output free ener gy of the loaded enzyme decayed almost linearly over the angular reaction c oordinate. Considering the threefold stepping and high activation barrier o f the driving motor proper, the rather constant output torque implied a sof t elastic power transmission between F-1 and F-O. It is considered as essen tial, not only for the robust operation of this ubiquitous enzyme under sym metry mismatch, but also for a high turnover rate of the two counteracting and stepping motor/generators.